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Promotion and Constraint of Adaptive Evolution in Cave-Dwelling Lineages

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Promotion and Constraint of Adaptive Evolution in Cave-Dwelling Lineages Promotion and constraint of adaptive evolution in cave-dwelling lineages Hilary Allison Edgington Sharon Center, Ohio Bachelor of Arts, The College of Wooster, 2010 A Dissertation presented to the Graduate Faculty of the University of Virginia in Candidacy for the Degree of Doctor of Philosophy Department of Biology University of Virginia May, 2015 i Dissertation Abstract Experiencing a novel environment is a common driver of evolutionary change. This change can be promoted by a variety of mechanisms and outcomes, such as novel selection, decreases in genetic variation due to founder effects, drift effects, and genetic admixture. Equally important are forces that impede or prevent change, including lack of suitable mutations, genetic correlations, developmental constraints, or antagonistic selection. A valuable system for studying questions related to evolutionary change following colonization of a novel habitat is the cave habitat, which has induced dramatic adaptive changes in many species that inhabit caves as a result of both adaptive and neutral forces. I studied the evolution of cave-dwelling salamanders, and in particular in the cave salamander, Eurycea lucifuga. Eurycea lucifuga is an evolutionary puzzle, inhabiting caves while having maintained brilliant coloration more typical of ancestral, surface dwelling ancestors. I first compared body shape among salamanders within Eurycea to examine the prediction from many previous studies that cave-dwellers are elongated relative to non- cave-dwellers. I found that terrestrial species were larger than aquatic species, and also that cave species had shorter tails relative to their body size than non-cave species. These results contrast with trends generally discussed in the cave literature, and reflect a need for explicit testing of how habitat impacts morphology in salamanders. I next investigated the phylogeographic history of Eurycea lucifuga and found that divergence among major lineages happened millions of years ago, with more recent expansion within each clade. This is similar to other cave-dwellers that show extreme morphological specialization to the subterranean climate. Our results do not support the idea that a lack ii of time underground acts as a constraint on adaptive evolution in this species. Lastly, I compared phenotypic differentiation in color traits with neutral genetic differentiation. The findings indicated that at small scales there is evidence of local differentiation in color relative to the neutral expectation. However, the spatial structuring of differentiation differs between the color phenotype and genotype. Population genetic analyses within a cave system indicated that migration likely occurs by surface corridors, suggesting that coloration may be maintained by a more substantial reliance on non-cave habitats than has been documented for this species. I concluded from these results that the phenotype of the cave salamander, Eurycea lucifuga, is greatly impacted by a relatively minor aspect of its ecology, and hypothesize that its non-cave morphology is selectively maintained by use of surface habitats. In general, this work emphasizes the need to examine trait change in a broad context, considering phylogenetics, ecology, and neutral processes. iii Acknowledgements Though it is impossible to name all of the people who have contributed to the completion of this dissertation, there are a few who require special recognition. First and foremost, I am deeply grateful to my advisor, Doug Taylor, who has contributed overwhelmingly to any professional and personal growth I experienced during my time in his lab. From my first semester in the department, Doug put a great deal of energy into helping me identify my proximate and ultimate goals, and then supporting my pursuit of them wholeheartedly. His enthusiasm for unraveling scientific puzzles and the care he has put into mentoring me are examples I hope to follow someday in my own lab. I am also indebted to my committee members, Bob Cox, Butch Brodie, Laura Galloway, and Dave Carr. Their guidance and support, as well as their critical evaluation of the design, execution, and presentation of these projects, have been invaluable, and I could not have asked for a better group of mentors. Bob Cox in particular has been an incredibly conscientious first reader, and consistently went above and beyond to ensure that I was on track, both scientifically and administratively. I greatly appreciate his patience and keen insight. There exists a group of people who, like the Cave Salamander, display an overwhelming preference for the subterranean habitat. None of the research I have conducted would have been possible if not for the assistance of cavers across the country, who gave up their time to assist me in accessing caves and collecting samples. Though I will never attain their level of enthusiasm for caving, being deep underground with these fine folks has made me acutely aware of how incredible the natural world is, and what a small part of it I inhabit. I am also very grateful for the assistance of wildlife iv professionals throughout the country for their assistance with cave access and permit processing. I have been fortunate to work in a lab composed of exceptionally talented members, past and present. This project would not exist were it not for Peter Fields who first introduced me to the Cave Salamander at trivia night five years ago, and whose patience with my ignorant questions has been truly admirable over the years. Colleen Ingram came along just as I was starting to know enough about phylogenetics to get into trouble with it, and aside from her invaluable help in that regard she has proved to be a great friend and collaborator. I owe a great deal to Andrea Berardi, who has been a wonderful friend and a great example for me during her time in the Taylor lab and beyond. I am particularly thankful for her assistance in developing the ideas for Chapter 3, as well as her keen editing eye and insightful comments. This effort would have been abandoned long ago were it not for the feedback, suggestions, distractions, and coaching from Corlett Wood, Brian Sanderson, Malcolm Augat, and Karen Barnard-Kubow. Their friendship has enriched my life in Charlottesville more than I can express, and I am excited to find out what amazing directions their lives will all take in the future. Finally, the amount of support I have received throughout this process from my parents, my sister, and her family continues to amaze and humble me. The value my parents place on being a life-long learner and their pursuit of that goal in their own lives has been a constant inspiration to me, and I could not have asked for a better environment in which to start my exploration of the natural world. I am incredibly grateful that in moving to Charlottesville I was able to move closer to my sister Margaret as her family v has grown and changed. Not only has Margaret been a constant example for me in her selfless concern for each person in her life and the strength she displays during turbulent times, she also spent a weekend caving with me at great mental and physical risk. Thank you all. vi TABLE OF CONTENTS Abstract……………………………...………………………………………. i Acknowledgements………………………………..………………………… iii Table of Contents…………………………………………….……………… vi Introduction……………………………………..…………………………… 1 Chapter 1: The phylogenetic history of body shape variation in salamanders of the Plethodontid genus Eurycea (Plethodontidae)…………….………….. 15 Figures and Tables…………………………………………...………. 33 Chapter 2: The phylogeography and population genetics of a cave-dwelling salamander, Eurycea lucifuga………………………………….…………….. 56 Figures and Tables………………………………...…………………. 84 Chapter 3: Varying color differentiation at multiple spatial scales in the cave salamander, Eurycea lucifuga (Plethodontidae)…...………………...……….. 97 Figures and Tables……………………………………………………. 130 Appendix A: Development and characterization of 19 microsatellite loci in the cave salamander, Eurycea lucifuga (Plethodontidae)….……………………. 145 1 Introduction Understanding the parameters that impact a species’ ability to adapt and survive in a novel environment has been crucial to evolutionary biology, conservation biology, and ecology (Bradshaw 1991; Charlesworth & Hughes 2000; Reed et al. 2003). Exposure to novel environments can come about primarily two ways: either a change occurs in a population’s current range, or there is dispersal and colonization of a new space. Perhaps the most ubiquitous example of these processes is the disruption of environment that accompanied glaciation in the Pleistocene, which not only altered the physiology and behavior of many species, but also dramatically impacted many species’ ranges (Avise 2000). There are many features of both populations and habitats that will make colonization more or less likely. Colonization success varies across species with differing biotic traits such as taxon, species, body size, and functional group (Eggleston et al. 1999), and is more likely in species that display omnivory, gregariousness, and asexuality (Ehrlich 1989; Lodge 1993). Features such as the type and size of a species’ abiotic habitat also impact colonization success (Eggleston et al. 1999). It has been suggested that some colonizers gain a benefit from preadaptation, for example an ability to use the widest range or commonest type of habitat (Thomas et al. 2001), or from phenotypic plasticity (Baldwin 1896; Ehrlich 1989; Holway & Suarez 1999). Once a novel environment has been experienced,
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